Speed-dependent modulation of wing muscle recruitment intensity and kinematics in two bat species

Abstract

Animals respond to changes in power requirements during locomotion by modulating the intensity of recruitment of their propulsive musculature, but many questions concerning how muscle recruitment varies with speed across modes of locomotion remain unanswered. We measured normalized average burst EMG (aEMG) for pectoralis major and biceps brachii at different flight speeds in two relatively distantly related bat species: the aerial insectivore Eptesicus fuscus, and the primarily fruit-eating Carollia perspicillata. These ecologically distinct species employ different flight behaviors but possess similar wing aspect ratio, wing loading and body mass. Because propulsive requirements usually correlate with body size, and aEMG likely reflects force, we hypothesized that these species would deploy similar speed-dependent aEMG modulation. Instead, we found that aEMG was speed independent in E. fuscus and modulated in a U-shaped or linearly increasing relationship with speed in C. perspicillata. This interspecific difference may be related to differences in muscle fiber type composition and/or overall patterns of recruitment of the large ensemble of muscles that participate in actuating the highly articulated bat wing. We also found interspecific differences in the speed dependence of 3D wing kinematics: E. fuscus modulates wing flexion during upstroke significantly more than C. perspicillata. Overall, we observed two different strategies to increase flight speed: C. perspicillata tends to modulate aEMG, and E. fuscus tends to modulate wing kinematics. These strategies may reflect different requirements for avoiding negative lift and overcoming drag during slow and fast flight, respectively, a subject we suggest merits further study.

Warm bodies, cool wings: regional heterothermy in flying bats

“…The extent to which muscles experience regional heterothermy in flying bats is striking because bat flight requires high limb cycling frequencies driven by fast and coordinated contraction [19,20] of the warm pectoralis and the cooler muscles distal to the shoulder. These distal muscles likely must also contract and relax at the wingbeat frequency, but temperature effects in the muscles may impair locomotor function.…”

Evolution of Flight Muscle Contractility and Energetic Efficiency

“…The resting sarcomere length of bat pectoral muscle is ∼2.2 μm and is similar to that of rat skeletal muscles ( Mathieu-Costello et al, 1992 ). A feature of bat flight is that the recruitment of pectoralis muscle fibers is modulated by flight speed similar to that of birds ( Konow et al, 2017 ). Power production is associated with changes in flight speed ( Hermanson et al, 1998 ).…”

“…Varied flight speeds of different bat species might be due to diverse fiber compositions. Pectoralis muscle of insect-feeding bats contains only non-fatigable fast oxidative-glycolytic fibers, whereas fruit-feeding bat pectoralis muscle contains multiple types of fiber ( Hermanson et al, 1998 ; Konow et al, 2017 ).…”

Wings as inertial appendages: how bats recover from aerial stumbles

“…We measured humeral elevation/depression as dorsoventral motion of the elbow relative to the shoulder. This variable is directly related to forces produced by contraction of the primary downstroke muscle, the pectoralis, and of the dorsal shoulder musculature that effects upstroke (Hermanson and Altenbach, 1985;Konow et al, 2017), and thus should directly reflect motor control of the shoulder joint. We used this angle to define wing stroke A B C y z Fig.…”